An RNA pseudoknot in the 3′ end of the arterivirus genome has a critical role in regulating viral RNA synthesis

Journal of Virology

Volumn 81, Issue 17, 2007, Pages 9426-9436

  Beerens, Nancy ^a   Snijder, Eric J ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

SINDBIS VIRUS NONSTRUCTURAL PROTEIN 4; VIRUS RNA;

ARTERIVIRUS; ARTICLE; EQUINE VIRAL ARTERITIS VIRUS; GENE SWITCHING; GENETIC CODE; LIFE CYCLE; MOLECULAR EVOLUTION; MOLECULAR INTERACTION; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROGENY; REGULATORY MECHANISM; RNA STRUCTURE; RNA SYNTHESIS; RNA TRANSLATION; SITE DIRECTED MUTAGENESIS; VIRION; VIROGENESIS; VIRUS GENOME; VIRUS NUCLEOCAPSID;

ANIMALS; ARTERITIS VIRUS, EQUINE; ARTERIVIRUS; BASE SEQUENCE; CELL LINE; CRICETINAE; GENETIC ENGINEERING; GENOME, VIRAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NUCLEIC ACID CONFORMATION; RNA, VIRAL; SEQUENCE HOMOLOGY, NUCLEIC ACID; TRANSFECTION; VIRUS REPLICATION;

ARTERIVIRUS; EQUINE ARTERITIS VIRUS; RNA VIRUSES;

EID: 34548160626     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00747-07     Document Type: Article

References (53)

1. Almazan, F., C. Galan, and L. Enjuanes. 2004. The nucleoprotein is required for efficient coronavirus genome replication. J. Virol. 78:12683-12688.
2. Baric, R. S., G. W. Nelson, J. O. Fleming, R. J. Deans, J. G. Keck, N. Casteel, and S. A. Stohlman. 1988. Interactions between coronavirus nucleocapsid protein and viral RNAs: implications for viral transcription. J. Virol. 62:4280-4287.
3. Beerens, N., and E. J. Snijder. 2006. RNA signals in the 3′ terminus of the genome of equine arteritis virus are required for viral RNA synthesis. J. Gen. Virol. 87:1977-1983.
4. Brierley, I., P. Digard, and S. C. Inglis. 1989. Characterization of an efficient coronavirus ribosomal frameshifting signal: requirement for an RNA pseudoknot. Cell 57:537-547.
5. den Boon, J. A., E. J. Snijder, E. D. Chirnside, A. A. de Vries, M. C. Horzinek, and W. J. M. Spaan. 1991. Equine arteritis virus is not a togavirus but belongs to the coronaviruslike superfamily. J. Virol. 65:2910-2920.
6. DeRijk, P., and R. DeWachter. 1997. RnaViz, a program for the visualisation of RNA secondary structure. Nucleic Acids Res. 25:4679-4684.
7. Enjuanes, L., F. Almazan, I. Sola, and S. Zuniga. 2006. Biochemical aspects of coronavirus replication and virus-host interaction. Annu. Rev. Microbiol. 60:211-230.
8. Gluick, T. C., R. B. Gerstner, and D. E. Draper. 1997. Effects of Mg2+, K+, and H+ on an equilibrium between alternative conformations of an RNA pseudoknot. J. Mol. Biol. 270:451-463.
9. Goebel, S. J., B. Hsue, T. F. Dombrowski, and P. S. Masters. 2004. Characterization of the RNA components of a putative molecular switch in the 3′ untranslated region of the murine coronavirus genome. J. Virol. 78:669-682.
10. Goebel, S. J., T. B. Miller, C. J. Bennett, K. A. Bernard, and P. S. Masters. 2007. A hypervariable region within the 3′ cis-acting element of the murine coronavirus genome is nonessential for RNA synthesis but affects pathogenesis. J. Virol. 81:1274-1287.
11. Gorbalenya, A. E., L. Enjuanes, J. Ziebuhr, and E. J. Snijder. 2006. Nidovirales: evolving the largest RNA virus genome. Virus Res. 117:17-37.
12. Hsue, B., T. Hartshorne, and P. S. Masters. 2000. Characterization of an essential RNA secondary structure in the 3′ untranslated region of the murine coronavirus genome. J. Virol. 74:6911-6921.
13. Hsue, B., and P. S. Masters. 1997. A bulged stem-loop structure in the 3′ untranslated region of the genome of the coronavirus mouse hepatitis virus is essential for replication. J. Virol. 71:7567-7578.
14. Huang, P., and M. M. Lai. 2001. Heterogeneous nuclear ribonucleoprotein A1 binds to the 3′-untranslated region and mediates potential 5′-3′-end cross talks of mouse hepatitis virus RNA. J. Virol. 75:5009-5017.
15. Jacobson, S. J., D. A. M. Konings, and P. Sarnow. 1993. Biochemical and genetic-evidence for a pseudoknot structure at the 3′ terminus of the poliovirus RNA genome and its role in viral RNA amplification. J. Virol. 67:2961-2971.
16. Koev, G., S. J. Liu, R. Beckett, and W. A. Miller. 2002. The 3′-terminal structure required for replication of barley yellow dwarf virus RNA contains an embedded 3′ end. Virology 292:114-126.
17. Kolk, M. H., M. van der Graaf, S. S. Wijmenga, C. W. A. Pleij, H. A. Heus, and C. W. Hilbers. 1998. NMR structure of a classical pseudoknot: interplay of single- and double-stranded RNA. Science 280:434-438.
18. Maines, T. R., and M. A. Brinton. 2001. Identification of cell proteins that bind to the SHFV 3′ (+)NCR. Adv. Exp. Med. Biol. 494:647-653.
19. Maines, T. R., M. Young, N. N. Dinh, and M. A. Brinton. 2005. Two cellular proteins that interact with a stem loop in the simian hemorrhagic fever virus 3′(+)NCR RNA. Virus Res. 109:109-124.
20. Mandal, M., and R. R. Breaker. 2004. Gene regulation by riboswitches. Nat. Rev. Mol. Cell. Biol. 5:451-463.
21. Masters, P. S. 2006. The molecular biology of coronaviruses, p. 193-292. In K. Maramorosch and A. Shatkin (ed.), Advances in virus research, 66. Academic Press, New York, NY.
22. Mirmomeni, M. H., P. J. Hughes, and G. Stanway. 1997. An RNA tertiary structure in the 3′ untranslated region of enteroviruses is necessary for efficient replication. J. Virol. 71:2363-2370.
23. Molenkamp, R., S. Greve, W. J. M. Spaan, and E. J. Snijder. 2000. Efficient homologous RNA recombination and requirement for an open reading frame during replication of equine arteritis virus defective interfering RNAs. J. Virol. 74:9062-9070.
24. Molenkamp, R., H. van Tol, B. C. Rozier, Y. van der Meer, W. J. M. Spaan, and E. J. Snijder. 2000. The arterivirus replicase is the only viral protein required for genome replication and subgenomic mRNA transcription. J. Gen. Virol. 81:2491-2496.
25. Nelson, G. W., S. A. Stohlman, and S. M. Tahara. 2000. High affinity interaction between nucleocapsid protein and leader/intergenic sequence of mouse hepatitis virus RNA. J. Gen. Virol. 81:181-188.
26. Novak, J. E., and K. Kirkegaard. 1994. Coupling between genome translation and replication in an RNA virus. Genes Dev. 8:1726-1737.
27. Nudler, E., and A. S. Mironov. 2004. The riboswitch control of bacterial metabolism. Trends Biochem. Sci. 29:11-17.
28. Olsthoorn, R. C., S. Mertens, F. T. Brederode, and J. F. Bol. 1999. A conformational switch at the 3′ end of a plant virus RNA regulates viral replication. EMBO J. 18:4856-4864.
29. Pasternak, A. O., A. P. Gultyaev, W. J. M. Spaan, and E. J. Snijder. 2000. Genetic manipulation of arterivirus alternative mRNA leader-body junction sites reveals tight regulation of structural protein expression. J. Virol. 74:11642-11653.
30. Pasternak, A. O., W. J. M. Spaan, and E. J. Snijder. 2006. Nidovirus transcription: how to make sense. J. Gen. Virol. 87:1403-1421.
31. Pasternak, A. O., E. van den Born, W. J. M. Spaan, and E. J. Snijder. 2001. Sequence requirements for RNA strand transfer during nidovirus discontinuous subgenomic RNA synthesis. EMBO J. 20:7220-7228.
32. Pleij, C. W. A. 1994. RNA pseudoknots. Curr. Opin. Struct. Biol. 4:337-344.
33. Pogany, J., M. R. Fabian, K. A. White, and P. D. Nagy. 2003. A replication silencer element in a plus-strand RNA virus. EMBO J. 22:5602-5611.
34. Puglisi, J. D., J. R. Wyatt, and I. Tinoco. 1990. Conformation of an RNA pseudoknot. J. Mol. Biol. 214:437-453.
35. Sawicki, S. G., and D. L. Sawicki. 1995. Coronaviruses use discontinuous extension for synthesis of subgenome-length negative strands. Adv. Exp. Med. Biol. 380:499-506.
36. Sawicki, S. G., D. L. Sawicki, and S. G. Siddell. 2007. A contemporary view of coronavirus transcription. J. Virol. 81:20-29.
37. Schelle, B., N. Karl, B. Ludewig, S. G. Siddell, and V. Thiel. 2005. Selective replication of coronavirus genomes that express nucleocapsid protein. J. Virol. 79:6620-6630.
38. Schuppli, D., J. Georgijevic, and H. Weber. 2000. Synergism of mutations in bacteriophage Q. beta RNA affecting host factor dependence of Q. beta replicase. J. Mol. Biol. 295:149-154.
39. Snijder, E. J., S. G. Siddell, and A. E. Gorbalenya. 2005. The order Nidovirales, p. 390-404. In B. W. Mahy and V. ter Meulen (ed.), Topley and Wilson's microbiology and microbial infections. Hodder Arnold, London, United Kingdom.
40. Snijder, E. J., Y. van der Meer, J. Zevenhoven-Dobbe, J. J. M. Onderwater, J. van der Meulen, H. K. Koerten, and A. M. Mommaas. 2006. Ultrastructure and origin of membrane vesicles associated with the severe acute respiratory syndrome coronavirus replication complex. J. Virol. 80:5927-5940.
41. Stohlman, S. A., R. S. Baric, G. N. Nelson, L. H. Soe, L. M. Welter, and R. J. Deans. 1988. Specific interaction between coronavirus leader RNA and nucleocapsid protein. J. Virol. 62:4288-4295.
42. Sudarsan, N., J. E. Barrick, and R. R. Breaker. 2003. Metabolite-binding RNA domains are present in the genes of eukaryotes. RNA 9:644-647.
43. van den Born, E., C. C. Posthuma, A. P. Gultyaev, and E. J. Snijder. 2005. Discontinuous subgenomic RNA synthesis in arteriviruses is guided by an RNA hairpin structure located in the genomic leader region. J. Virol. 79:6312-6324.
44. van der Meer, Y., H. van Tol, J. Krijnse Locker, and E. J. Snijder. 1998. ORF1a-encoded replicase subunits are involved in the membrane association of the arterivirus replication complex. J. Virol. 72:6689-6698.
45. van Dinten, L. C., J. A. den Boon, A. L. M. Wassenaar, W. J. M. Spaan, and E. J. Snijder. 1997. An infectious arterivirus cDNA clone: identification of a replicase point mutation that abolishes discontinuous mRNA transcription. Proc. Natl. Acad. Sci. USA 94:991-996.
46. Verheije, M. H., R. C. L. Olsthoorn, M. V. Kroese, P. J. M. Rottier, and J. J. M. Meulenberg. 2002. Kissing interaction between 3′ noncoding and coding sequences is essential for porcine arterivirus RNA replication. J. Virol. 76:1521-1526.
47. Williams, G. D., R. Y. Chang, and D. A. Brian. 1999. A phylogenetically conserved hairpin-type 3′ untranslated region pseudoknot functions in coronavirus RNA replication. J. Virol. 73:8349-8355.
48. Wyatt, J. R., J. D. Puglisi, and I. J. Tinoco. 1990. RNA pseudoknots: sStability and loop size requirements. J. Mol. Biol. 214:455-470.
49. Yu, W., and J. L. Leibowitz. 1995. A conserved motif at the 3′ end of mouse hepatitis virus genomic RNA required for host protein binding and viral RNA replication. Virology 214:128-138.
50. Yu, W., and J. L. Leibowitz. 1995. Specific binding of host cellular proteins to multiple sites within the 3′ end of mouse hepatitis virus genomic RNA. J. Virol. 69:2016-2023.
51. Zhang, G. H., J. C. Zhang, and A. E. Simon. 2004. Repression and derepression of minus-strand synthesis in a plus-strand RNA virus replicon. J. Virol. 78:7619-7633.
52. Zuker, M. 1989. On finding all suboptimal foldings of an RNA molecule. Science 244:48-52.
53. Zuker, M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31:3406-3415.